Download Competition for feeding in waders: a case study in an

 Springer 2005
Hydrobiologia (2005) 544:155–166
DOI 10.1007/s10750-005-0541-6
Primary Research Paper
Competition for feeding in waders: a case study in an estuary of south
temperate Europe (Mondego, Portugal)
Tiago Múrias Santos1,*, João Alexandre Cabral2, Ricardo Jorge Lopes1, Miguel Pardal3,
João Carlos Marques3 & John Goss-Custard4
1
CIBIO-UP, Campus Agrário de Vairão, 4485-661 Vairão, Portugal
CETAV, Laboratório de Ecologia Aplicada, Departamento de Cieˆncias Biológicas e Ambientais, Universidade de
Trás-os-Montes e Alto Douro, 5009-911 Vila Real, Portugal
3
IMAR – CIC, Universidade de Coimbra, 3004-517 Coimbra, Portugal
4
CEH – Winfrith Technology Centre, Dorchester, Dorset DT2 8ZD, United Kingdom
(*Author for correspondence: Tel.: +351-223401497, Fax: +351-223401511, E-mail: [email protected])
2
Received 16 May 2003; in revised form 15 December 2004; accepted 12 January 2005
Key words: competition, feeding, waders, habitat loss, Portuguese estuary
Abstract
The loss of feeding areas may pose a threat to many wintering waders because increased competition arising
from reduced foraging space may force birds either to emigrate or to die. This has been demonstrated to
occur in northwest European estuaries, but virtually no studies have been performed in the estuaries of
southern Europe, where the loss of supratidal habitats (salines and saltmarshes), rather than intertidal
habitats, are currently the main threat to waders’ habitats. If these habitats are lost, waders may be forced
to move to the intertidal mudflats, perhaps increasing competition between individuals and ultimately
leading to starvation or emigration. We tested this hypothesis in the Mondego estuary, a small estuary on
Portugal’s west coast, which is presently under heavy human pressure. We used indirect methods to test for
the occurrence of both components of intra-specific competition: interference and prey depletion. We found
no evidence that either interference or depletion competition was occurring at present, either on the
mudflats or in the salines. Overall, the results suggest that the intertidal mudflats may still be able to
accommodate birds displaced from the destroyed supratidal salines, but modelling is required to predict the
effect that the combined loss of feeding area and foraging time that this would entail would have on their
fitness, and thus numbers.
Introduction
The loss of feeding places in an estuary may pose a
problem for the waders that usually feed there.
While birds may eventually leave the area, it is
expected that their first reaction would be to
redistribute themselves within the estuary (GossCustard & Durell, 1990). The immediate consequence of redistribution following habitat loss is
an increase in the densities of birds feeding in those
areas that remain (Goss-Custard & Durell, 1990).
As densities rise, competition between birds may
increase, leading to a reduction in intake rate. At a
certain point as competition intensifies, emigration
and/or mortality rates also begin to increase,
whereupon they become density-dependent. From
this point on, further habitat loss or deterioration
will increase emigration and/or mortality rates,
and the population size will decrease (Goss-Custard & Durell, 1990; Goss-Custard et al., 1996). As
156
stressed by Goss-Custard & West (1997), the
moment at which this point is reached is what
really matters as, when it is passed, it ultimately
leads to a reduction in bird numbers.
In north European estuaries, the direct removal
of intertidal areas for industrial and urban construction is reported as the major cause of habitat
loss (Smit et al., 1987; Schekkerman et al., 1994).
This seems not to be the case in the southern
European estuaries, at least those on the Atlantic
coast of Portugal. Here, habitat loss is mainly due
to the destruction and/or conversion of supratidal
habitats, such as artificial saltpans, or salines (e.g.,
Rufino & Neves, 1992). Portuguese salines are
usually regarded as mainly providing supplementary feeding over high-water, on the assumption
that this habitat is less suitable than the mudflats
for most waders, although this may depend on the
species and/or the time of the year considered
(Rufino et al., 1984; Múrias, et al., 1997, 2002;
Luı́s, 1999; Lopes et al., 2001). In the Mondego
estuary (western Portugal), for example, up to
42% of the total number of waders present can be
found feeding in the salines at low-water, irrespective of the season, against some 70% at highwater (Múrias et al., 2002). The lack of winter
management of this habitat also causes many
ponds to be flooded from October to March, thus
preventing their use by birds over that period
(Múrias et al., 1997). Nevertheless, the salines may
still play an important role by providing both extra
feeding places and extra feeding time at low-water
and at high-water (Múrias et al., 2002). Consequently, their loss may be detrimental to many
species.
In the Mondego, as in other Portuguese estuaries, there have been increasing losses of salines
over the last decade (Múrias, 1997; Lopes et al.,
2001; Múrias et al., 2002). The effects, if any, that
these losses may already have had on the waders of
the Mondego estuary have not been monitored,
however. This paper, therefore sets out to predict
whether a continuing loss of salines would have an
impact on the birds through intensifying competition. We do this by thinking of a scenario in
which all existing salines have been rendered
unusable by waders so that all birds in the estuary
can only feed on the intertidal mudflats: other
supratidal habitats (ricefields, fishfarms) are
unsuitable for feeding or cannot be regularly used
by waders (Múrias et al., 1997; Lopes et al., 2001).
This scenario would affect the feeding conditions
of the birds in two ways. It would remove feeding
areas in the salines, thereby reducing the total
quantity and area of food available to the birds
over low-water. It would also remove a source of
food that is used over high-water by birds that,
over low-water, feed either in the salines or on the
inter-tidal flats of the estuary itself. It would
therefore reduce the amount of time available to
all birds for feeding from its present level of
12.15 h/tidal cycle to ca. 8 h/tidal cycle; i.e., the
time for which the intertidal mudflats are exposed.
In this study, we try to assess whether such
reductions in food supply would make it more
difficult for birds to survive the winter in good
condition, because the birds on the mudflats are
already subjected to intra-specific competition for
food. It is already well-known that intra-specific
competition can occur in wintering waders and can
take two forms: (a) interference while feeding and
(b) prey depletion, both of which can reduce intake
rate (Goss-Custard, 1980). This paper is only
concerned with testing whether either, or both,
forms of competition occur in this particular system. If one or both forms of competition were to
be detected in this system, one would expect further habitat loss to intensify it and perhaps lead to
density-dependent reductions in overwinter survival rate and/or poorer body condition at the time
of the spring migration (Goss-Custard & Durell,
1990). This outcome would put in danger the longterm survival of wader populations in the Mondego estuary.
Study area
The Mondego estuary is located on the west coast
of Portugal (4008¢ N, 850¢ W) and is presently
about 7 km long by 2–3 km wide. During the main
study period (1993–1995), it comprised a total area
of wetland habitat of approximately 1131 ha
(Múrias et al., 1997). In the seaward part, the river
divides into two arms surrounding an alluvialformed non-tidal island, the Morraceira (Fig. 1).
Of the total area of wetlands available for waders,
only 134 ha (11.8%) were intertidal. The remainder consisted of saltmarshes (5.5%) and humanmade or modified supra-tidal habitats: salines
157
Figure 1. The study area in the south arm of the Mondego
estuary, showing the sediment types and the 12 census sub-areas
that were combined to form the three main areas, ‘Gala’ (G),
‘Armazéns’ (A) and ‘Pranto’ (P). The three points from which
the birds were counted (1,2, 3) in the south arm are also shown,
along with the 16 transects used for the invertebrate sampling.
(27%), fish-farms (17%) and channels (38.7%)
(Múrias et al., 1997). From 1996 to 2001, an
additional 96 ha of mud and sandflats were created in the north arm, as a consequence of
dredging works associated with the enlargement of
the Figueira da Foz harbour (Lopes et al., 2001).
However, the percentage of birds of the studied
species that used these areas was only 6–14%, so
they were not included in the calculations.
The mudflats and salines are the main lowwater feeding areas in the estuary. The channels
sometimes provide low-water feeding sites, but
they are mostly used during the autumn migration
period. At high-water, most birds move to the
salines where many continue feeding (Múrias
et al., 1997; Lopes et al., 2001). Ricefields and
fishfarms may also be used through the whole tidal
cycle as feeding areas. However, their use is
constrained by their management regime. The
ricefields are used only in spring and by a limited
range of species, whereas the fishfarms are used in
those brief periods, usually in autumn, when they
are emptied for maintenance (Múrias, 1997).
Despite the small area of the intertidal mudflats,
there was an appreciable variation in the type of
sediment present. The flats adjacent to the margins
of the south arm of the Morraceira island were
made-up of finer sediments, while the central banks
consisted mainly of coarse-grained sediments (sand
or muddy-sand) (Cunha & Dinis, 2002). Based on
these differences in the sediment composition, it
was possible to subdivide the estuary into 12 discrete sub-areas (Fig. 1), naturally delimited by
channels and creeks. The average size of these areas
was 10.02 ± 11.8 (SD) ha (range: 0.7–27.1 ha). A
dense Spartina spp. marsh was present alongside
the island, with sparse meadows occurring downstream. The duration of the exposure time in different parts of the intertidal zone varied by only 0.5
– 1 h on an average high-tide of 0.8 m.
The salines were in the Morraceira Island and
along the left bank of the south arm, and all were
of the traditional type. A typical saline in the
Mondego is formed by a set of small ponds
(storage, evaporation and preparation ponds) of
decreasing depth (20 cm to 2–3 cm) and increasing
salinity, connected by drainage channels and sluices and linked to the river through a reservoir 80
cm deep (Múrias et al., 2002). The average area of
a saline in this estuary is 4.0 ha. Storage and
evaporation ponds were the preferred feeding
places for waders (Múrias, 1997).
Methods
Field methods
The study was restricted to the three species
most likely to be affected by competition due to
their high abundance and widespread distribution: Kentish Plover Charadrius alexandrinus,
Ringed Plover Charadrius hiaticula and Dunlin
Calidris alpina.
Interference competition
Following the logic of Goss-Custard et al. (1982),
we predicted that, if interference competition was
158
acting in this system, the proportion of the total
estuary population that fed in a preferred habitat
over low-water would decline as total numbers
increased. With few competitors present, all the
birds could feed in the most preferred sites without
too much interference. But as the total numbers
increase, interference would intensify, eventually
making it more profitable for some birds to move
to other less preferred sites within the estuary. The
competition hypothesis might also predict that, as
the total number of birds in the estuary increases,
an increasing proportion would be forced to feed
in the salines over high-water. This is because
increased competition over low-water would make
it more difficult for some birds to get all the food
they need when the tidal flats are exposed, and so
they continue to feed at high-water. Censuses,
therefore, provided the main data with which to
test for the presence of interference competition.
The number of each species feeding in each of
the 12 sub-areas of the estuary mudflats and a
large sample of 39 salines (90.6% of the total
number) in the Morraceira island, were counted 1–
2 times a month with 10 · 50 binoculars and a 20–
60 · 50 telescope. For the mudflats, counts were
made from three fixed positions along the south
arm (Fig. 1). In the salines, a car was used to
follow a fixed route. All counts were made within
2 h of dead water on spring tides. A total of 102
counts in the south arm mudflats and in the salines
at low water, and 12 counts in the salines at high
water, were available for the period 1993–2000. To
test for the occurrence of interference competition
up to 33 counts at low water in the build-up phase
(July–December) for the years 1993–1994 and
1996–2000, and 12 counts at high-water for the
same months, for 1993–1994, were used. Additionally, 7 winter counts (late November–March)
from 1993–1994 were used in the study of prey
depletion.
All waders seen on the mudflats were counted
and the boundaries of their flocks plotted on a
map, drawn from aerial photographs. The birds
present in the salines were counted next day. It was
assumed that all the birds present fed in the areas
where they were observed, even if they were not
feeding at the time they were counted. The maps of
bird flocks were superimposed on the map of the
sub-areas, allowing the allocation of each flock (or
part of it) to a given sub-area. Whenever a flock
was spread over several sub-areas, bird numbers
were assigned to each sub-area in proportion to
the respective area occupied by the flock. Counts
were obtained this way for each sub-area but, in
the final analysis, they were combined to form
three main areas, named ‘Gala’, ‘Armazéns’ and
‘Pranto’.
Depletion
Due to logistic constraints, it was not possible to
sample all the 12 sub-areas to measure the overwinter rates of prey depletion. In October 1994, a
series of transects were marked out in each of the
three main feeding areas (six transacts were placed
in ‘Gala’, four in ‘Armazéns’ and six in ‘Pranto’).
Each transect in areas ‘Gala’ and ‘Pranto’ contained five regularly spaced sampling points,
marked with bamboo stakes (Fig. 1). In area
‘Armazéns’, due to characteristics of the terrain,
the four transects from downstream to upstream
had, respectively, 5, 11, 18 and 6 sampling points.
A total of 90 sampling points were used. In late
November and early March, one sample was taken
at each sampling point in each transect using a
core of 95 cm2 in area and 5 cm deep. The samples
were taken to the laboratory, washed and sieved
through a 0.5 mm mesh, and stored in 4% neutralised formol. The collected organisms were later
separated, preserved in 70% alcohol and identified
and counted under a binocular microscope.
The prey species selected were the mobile gastropod Hydrobia ulvae and several, mostly sedentary, small worms (polychaetes and oligochaetes).
Due to their abundance in the estuary, the small
polychaete species Alkmaria romijni (ex-Amage
adspersa) and Streblospio shrubsolii were treated
separately. Hydrobia were divided into two groups
roughly corresponding to (i) the small, and
presumably less profitable, size-classes <1.5 mm
in length, and (ii) the larger, and presumably more
profitable, size-classes >1.5 mm (Goss-Custard
et al., 1991).
Data analysis
Interference competition
In order to test for the presence of interference, the
proportion of each species in each particular
159
habitat or area was regressed against the total
number of birds in the estuary during the build-up
phase (late July–December), when interference
competition might be expected gradually to
intensify (Goss-Custard et al., 1982). We considered both the intertidal areas and the salines as
being potentially preferred areas where interference competition might occur. In fact, the salines
had previously been considered as providing
mostly supplementary feeding (Múrias, 1997;
Múrias et al., 2002), but this assumption had never
been formally tested.
Due to differences between areas in size, sediment composition and degree of disturbance by
people, each of the three main intertidal areas was
separately analysed. The analyses were performed
for each species and area (salines and intertidal
areas) at low-water, and for the salines at highwater.
As bird numbers increased steadily throughout
the build-up phase, the total numbers on the estuary and the number of days elapsed since July 15th
were closely correlated. This raises the possibility
that different seasonal patterns of change in the
food supply in the three areas could confound with
bird numbers, thus making interpretation of the
results difficult. However, the food supply in the
three areas co-varied in parallel over the winter (see
below), suggesting that the relative quality of the
three feeding areas would not have changed over
the build-up phase. The collinearity of the total
number of days elapsed is not regarded, therefore,
as an hinderance to interpreting results.
Disturbance of birds by people is frequent on
the intertidal flats (e.g., Davidson & Rothwell,
1993) and perhaps on the salines. In the Mondego
estuary, significant disturbance by people – baitdiggers – was only observed in the intertidal area
‘Gala’. To test for a possible effect of disturbance
on bird distribution, the numbers of birds in ‘Gala’
were regressed against the number of people
present during the build-up phase. If birds had
been disturbed away from the Gala by people, a
negative relationship should be present. Numbers
were not influenced by human disturbance in any
of the three species studied (F1,25 ¼ 0.88,
F1,28 ¼ 0.001, F1,28 ¼ 0.66, ns; for Kentish Plover,
Ringed Plover and Dunlin, respectively), suggesting that bird distribution at the spatial scale considered was unaffected by the presence of people.
In order to conform with the assumptions of
the parametric
tests, proportions were transformed
pffiffiffi
(arcsin n). The counts using the birds in salines at
high-water excluded those birds that were also
present in the salines over low-tide (i.e throughout
the tidal cycle), as well as those birds that were
roosting at high-tide. In this way, we were able
only to consider the birds that had fed over lowwater on the mudflats but then continued feeding
over high-water in the salines.
Depletion
In addition to the interference competition, food
depletion over the winter could also lead to competition between birds due to a reduction in the
standing crop of the food supply. As no recruitment and little growth usually occurs over the
winter in most northern-temperate estuaries
(McLusky, 1989), the invertebrate food resources
of shorebirds there usually decline from autumn to
spring through depletion by waders and other
predators and through a variety of other causes of
loss (e.g., gales). If waders contribute a great deal
to the prey loss, increased bird densities in an area
will necessarily increase the rate of prey depletion,
potentially decreasing intake rates and thus
intensifying competition (Goss-Custard, 1980).
But in the Mondego estuary, as in many estuaries
of southern Europe, recruitment and, particularly,
growth continues in several species throughout
the winter (Pardal, 1998; Cardoso et al., 2002;
Dolbeth et al., 2003). Although winter growth of
invertebrates in this estuary is much lower than its
spring-summer equivalent (M. Pardal, personal
communication) this could, nevertheless, prevent
depletion by birds by reducing the standing crop of
their food supply, so preventing competition
through depletion from occurring.
We first investigated whether the standing crop
biomass of the prey did decrease over the winter or
whether it remained constant, or even increased,
because prey losses from all sources were replaced
by recruitment and growth. But to predict whether
an increased density of waders would decrease
their food supply over the winter, we also needed
to know whether the birds currently removed a
significant proportion of the standing crop. We
therefore compared the total energy requirements
of the birds over the winter with the prey standing
crop at various stages throughout the winter.
160
Overwinter prey loss. Whether the food supply
was reduced over the winter was investigated by
comparing the biomass of prey species (Table 1) in
early winter (November), before the main arrival
of wintering birds, with those in early spring
(March), after most wintering birds had gone, but
before the arrival of spring migrants. If prey
abundance was reduced significantly, prey depletion could have been important because it would
imply that prey losses were not replaced by
recruitment and growth.
Total prey removed. The simple comparison of
biomass at the start and end of winter, however,
does include any effect of other non-shorebird
predators on prey abundance. In order to provide
a measure of depletion by the study birds themselves, we compared the total energy of the main
prey available in the feeding areas across the
winter with the energy requirements of all the
birds. By using the monthly values for the prey
standing stocks, the influence of prey growth and
recruitment between two consecutive months was
largely taken into account.
The total biomass of all the intertidal invertebrate species present at the start of winter was
considered to be the food supply of the shorebirds.
Data on the biomasses of invertebrates (g m)2)
were obtained for the months of November 1993
through March 1994 (Pardal, 1998; Cardoso et al.,
2004). We assumed that all prey size-classes were
taken by waders. In fact, it is likely that, for some
species/groups (e.g. Nereis (Hediste) diversicolor),
only the larger size-classes were actually taken
Table 1. Contribution of each invertebrate taxa to the overall
biomass (expressed in energy equivalents, kJ m-2) present in the
intertidal flats of the Mondego estuary, between November
1993 and March 1994
Polychaeta
Average monthly
%Contribution to
biomass (±SD)
total biomass
14.18 ± 9.39
2.0
Bivalvia
110.23 ± 45.86
15.6
Hydrobia ulvae
521.46 ± 73.43
73.7
Other Gastropoda
18.01 ± 9.63
2.6
Crustaceans
49.08 ± 23.81
6.9
1.19 ± 1.18
707.22 ± 89.47
0.2
100.0
Other
All taxa
(Pienkowski, 1982; Goss-Custard, 1984; GossCustard et al., 1991; Moreira, 1994a, b; Piersma,
1996). Therefore, our measures may have overestimated the energy available to shorebirds from
these groups. These values, thus, provide a maximum measure of the total gross energy available to
waders in the mudflats (Evans et al., 1979).
Although the diets of some wader species are
still poorly studied in the Mondego estuary, Lopes
et al. (1998) and Cabral et al. (1999) presented
some data on the most numerous species: Dunlin,
Ringed Plover, Kentish Plover and Grey Plover
Pluvialis squatarola. According to these authors,
these species feed mostly upon polychaetes
(35–67% occurrences in feacal pellets), Hydrobia
ulvae (33–74%), Scrobicularia plana (2.9–22%)
and small crustaceans (11–44%). Two other
important wader species using the estuary in
winter are the Black-tailed Godwit Limosa limosa
and the Avocet Recurvirostra avosetta. Unfortunately, there are no dietary data available for these
species. We have assumed that godwits preyed
mostly upon bivalves (Scrobicularia plana), and
Avocets ate mostly polychaetes, as they do in the
Tagus estuary (Moreira, 1994b; 1995).
The Total Gross Biomass (TGB) of invertebrates present in a month per unit area
(g AFDM m)2) was calculated as
TGB ¼ RBij
ð1Þ
where Bij is the average biomass density
(g AFDM m)2) of the ith intertidal invertebrate
species, according to the data obtained from Pardal
(1998) and Cardoso et al. (2004), in month j. The
Total Gross Energy (TGE) present on a given month
per unit of area (kJ m)2) was then calculated as:
TGB ¼ RðBij 21Þ
ð2Þ
where 21 represents the average calorific value of
1 g of ash-free dry weight (McLusky, 1989; Zwarts
& Wanink, 1993)
The gross energy requirements of each bird
species were calculated from the total bird-days
present in each month, as calculated from the
winter counts for November–March 1993–1994
(see Field methods). The Total Gross Biomass
Consumed (TGBC), in kJ m)2 month for each
species was calculated as:
161
TGBC ¼ BD gross FMR n1; 340; 000
ð3Þ
where BD, the number of bird-days, is N (average
number of birds per month) · 30 days, and FMR
is the Field Metabolic Rate, the gross energy daily
expenditure of a bird involved in ‘normal’ activities (feeding, roosting, preening, flying). FMR was
calculated using Nagy et al. (1999) equation for
a range of species of Charadriiforms, using
the double-labelled water method (D2O):
FMR ¼ 8.13 · BM0.77, expressed in kJ bird day)1.
The value 1,340,000 is the total area, in m2, of the
intertidal mudflats. Body masses (BM) were
obtained from Cramp & Simmons (1983), using
the appropriate values for the latitude and time of
year (Table 2). TGBC values were divided by 0.80
to take assimilation efficiency into account
(Klaassen et al., 1990).
Results
Interference competition
There was no evidence to suggest that interference
competition occurred amongst birds feeding over
Table 2. Energy requirements (Total Gross Biomass consumed) of the wader species present in the winter of 1993–
1994 on the Mondego estuary
Species
Body
FMR
Average
weight
(kJ day)1)
monthly
bird-days
(kg)
(± SD)
Kentish Plover
50
93
2688 ± 2690
Ringed Plover
Grey Plover
50
190
93
232
2568 ± 1859
4320 ± 1523
Numenius spp.1
560
484
138 ± 137
Black-tail.Godwit
290
309
3876 ± 8617
Comm. Sandpiper
50
93
156 ± 130
140
188
168 ± 282
Dunlin
50
93
16128 ± 11596
Little Stint
30
66
186 ± 416
Avocet
All species
240
272
14802 ± 8571
4053 ± 6001
Knot
FMR is calculated from the bird body masses shown, using the
allometric formulae of Nagy (1999) and assuming an assimilation efficiency of 80% (Klaassen et al., 1990).
1
Numenius arquata and N. phaeopus. The values for these
especies were averaged in all cases.
Figure 2. Example of the type of relationship between the total
population of a target species (Dunlin) present in the estuary
and salines combined and the percentage of birds in each of the
main intertidal areas and the salines at low-water. Data are for
the periods of July to early December of 1993–1995 and 1996–
2000 (low-water).
the low tide in any of the three mudflat areas. For
Kentish Plover and Ringed Plover, the proportion
(arcsin-transformed) of birds in each intertidal
area and in the salines at low-water, did not decrease significantly as total numbers in the estuary
increased (for ‘Gala’ ‘Armazéns’,’Pranto’ and salines, respectively: Kentish Plover: r2 ¼ 0.0007,
r2 ¼ )0.02, r2 ¼ 0.02 and r2 ¼ 0.09, n ¼ 32, ns;
162
Figure 3. Change in numbers (average of the transects), from
November 1993 to March 1994, in the densities of several
groups of polychaetes and oligochaetes (above) and percentage
changes of different size-classes of Hydrobia ulvae (below) in
three main areas of mudflats, and all areas combined, in the
Mondego estuary.
Ringed Plover: r2 ¼ 0.08, r2 ¼ )0.09, r2 ¼ )0.02
and r2 ¼ )0.009, n=32, ns). The proportion of
Dunlin even increased in one area (‘Armazéns’,
r2=0.19, n ¼ 32, p < 0.008), but showed no significant trend in the other two and in the salines
(r2 ¼ )0.03, r2 ¼ )0.0002 and r2 ¼ )0.03, n ¼ 32,
ns; for ‘Gala ‘, ‘Pranto’ and salines, respectively).
The data for Dunlin are shown in Figure 2 to
illustrate the distribution of the data points in
these analyses.
There was no evidence, either, that the proportion of birds in the salines over high-water decreased
with total numbers, for any species r2 ¼ 0.25,
r2=)0.14, r2 ¼ 0.31, n ¼ 12, ns; for Ringed Plover,
Kentish Plover and Dunlin, respectively).
Depletion
Overwinter reduction in prey abundance
There was no evidence of an overwinter reduction in
the densities of polychaetes and oligochaetes
between November and March, as would be
expected if waders exerted a strong predation
pressure on their food supply (Fig. 3, top). Indeed,
the abundance of the individual species or groups of
worms, singly and in combination, showed a
pronounced increase from November to March
(Kruskal–Wallis test: v22.33 ¼ 17.03, p < 0.001,
v22.33 ¼ 12.89, p < 0.003, v22.33 ¼ 13.34, p < 0.003
and v22.33 ¼ 18.61, p < 0.0001 for Alkmaria sp.,
Streblospio sp., Oligochaetes and total Polichaetes,
respectively). Significant spatial differences in the
magnitude of the increase only occurred in Streblospio and Oligochaetes, which exhibited higher
between-month differences in the ‘Pranto’ area, as
compared to the two downstream areas
(v22.16 ¼ 11.49, p < 0.003, and v22.16 ¼ 8.72,
p < 0.01, for the two groups, respectively).
The small decrease in the abundance of all sizeclasses of Hydrobia combined that was observed
across all areas was not statistically significant
(v22.32 ¼ 0.006, ns) (Fig. 3, bottom). However, the
seasonal changes in abundance differed between
size-classes. The density of the larger individuals
across all areas significantly increased from
November to March (v22.32 ¼ 7.07 p < 0.008)
whereas the density of the smaller ones did not
change (v22.32 ¼ 0.57, ns). There were no significant differences between the three areas in densities, both for each size class separately
(v22.16 ¼ 3.05, ns and v22.16 ¼ 3.31, ns, for larger
and small Hydrobia, respectively) and for all sizeclasses combined (v22.16 ¼ 2.92, ns).
Energy requirements of the birds
The comparison of the birds’ energy requirements
with the biomass (in kJ m)2) standing stock of the
main prey species present in each month from
November 1993 to March 1994 is shown in Tables
2 and 3. The comparison was made on a monthly
basis, rather than for the winter as a whole, because of the evidence that food abundance often
increased during the winter. Birds removed each
month only 0.77–3.41% of the total gross biomass
that was present in that month.
The low values of biomass removed may have
been due to the overwhelming predominance of
Hydrobia in the macro-invertebrate biomass
(Table 1). If the most preferred prey were actually
polychaetes, the impact of shorebirds on their food
supplies each month would have been greater
163
(2.26–13.42%) (Table 3). If, on the other hand,
Hydrobia was the most important prey, as
suggested by Lopes et al. (1998) and Cabral et al.
(1999), some 37% of the total and renewing
biomass would have been removed by birds during
the whole winter. However, given Hydrobia’s thick
and indigestible shell (Zwarts & Blomert, 1990),
this might be less likely.
Discussion
Some studies that have attempted to predict the
consequences of habitat loss for waders in their
wintering or staging sites have focussed on food
depletion and paid rather little attention to interference competition (e.g., Evans et al., 1979; Meire
et al., 1994). However, competition in the feeding
areas may arise from both these feed-back processes (Goss-Custard, 1980) and detailed studies
may be required to establish the relative importance of each (Goss-Custard et al., 2001; GossCustard et al., 2003). An attempt was made to
assess the occurrence of both processes in the
Mondego estuary.
Neither the studies of the distribution of birds
over the intertidal feeding areas and salines at low
tide nor of the proportion of birds using the salines
over high tide provided any evidence that interference competition occurred. If it did occur, its
effects must have been operating at such a low
level that it did not significantly affect the intake
rates and behaviour of the birds. This conclusion is
further supported by the lack of a relationship
between bird density and pecking rates – which in
charadrids are roughly correlated (Pienkowski,
1982) – that was found in a previous study in the
Mondego estuary by Cabral et al. (1999). Indeed,
in Kentish Plover, the pecking rate even increased
with increasing density (Cabral et al., 1999). Further evidence that interference competition was
slight or absent in the Mondego intertidal areas is
that the density of none of the three species
reached the threshold values of 50–300 birds/ha at
which, in waders, interference begins to occur
(Yates et al., 1999; Triplet et al., 2000; Stillman
et al., 2002). During this study, the maximum
density recorded in any species barely reached 10
birds/ha (Dunlin, in December 1993). However,
the birds were, at any one time, aggregated into
only a small part of the area, so their effective
density may have exceeded the threshold densities.
For birds taking small prey, the interference
threshold density would be in the range 150–300
birds ha, possibly more (Stillman et al., 2002). So,
for the effective bird density to exceed this
threshold, birds would have had to occupy at any
one time less that 1/15th of the whole area (Stillman et al., 2002). In fact, for all studied species,
the birds were much more spread out than this
Table 3. Total biomass taken in each month of the winter by all species of waders in the estuary of Mondego during the winter of
1993–1994, in relation to the standing crop biomass (in energy equivalents, kJ m)2) present in each month of (a) all invertebrate species
that can potentially be eaten, (b) all invertebrate species excluding Hydrobia ulvae and (c) only Hydrobia ulvae
Month
Number
Total gross
of bird-days
biomass
(kJ m)2)
Energy consumption
Including all taxa
Excluding Hydrobia ulvae
Only Hydrobia ulvae
Standing crop %Biomass
Standing crop %Biomass
Standing crop %Biomass
(kJ m)2)
(kJ m)2)
(kJ m)2)
taken
taken
taken
November
43200
4.63
598.88
0.77
204.53
2.260
394.36
1.17
December
43950
10.71
781.03
1.37
255.95
4.18
525.08
2.04
January
71400
16.16
706.03
2.29
182.21
8.87
523.83
3.08
February
50340
21.86
640.84
3.41
162.85
13.42
477.99
4.57
March
16260
23.11
809.33
2.86
213.33
10.83
596.00
3.88
15.29 ±
707.22 ±
2.14 ±
203.77 ±
503.45 ±
2.95 ±
Mean ± S.D 45030 ±
19721
7.74
89.47
7.74
35.19
7.91 ±
4.63
The average values (± 1 standard-deviation of the mean) for the whole period are also given.
74.16
1.37
164
over their feeding areas throughout the whole of
the low-water period. Significant aggregation only
occurred 1–2 h before high-water, by which time
many birds had already left the interidal areas for
their supratidal refuges and most of those
remaining had stopped feeding. So, even under
these circumstances, it is very unlikely that bird
density was high enough for the effective density
threshold to be reached. There is therefore little
reason to suspect that interference would have
affected the intake rates of most waders.
Depletion of the main food supplies of waders in
intertidal areas also seems to have been negligible.
Indeed, the densities of the probably most important prey types, small polychaete worms and larger
Hydrobia, actually increased from November to
March, despite the depletion by birds. This was
presumably due to over-winter growth and/or
reproduction of the invertebrates in this warmtemperate latitude estuary, in contrast to its
northern counterparts. Pardal (1998) found that
the polychaete Alkmaria romijni showed continuous growth throughout the winter. As for Hydrobia, the decrease in small-sized Hydrobia, and
corresponding increase in the number of large-sized
ones, suggests that growth also occurred in this
species in the Mondego estuary over the winter.
The conclusion that overwinter prey depletion
was negligible was reinforced by the comparison
between the birds’ energy requirements and the
standing stocks of the prey. Biomass consumption
by birds was very small, being generally less than
8% over the whole winter, even when Hydrobia,
the dominant species in the flats, was excluded.
This value is well below the typical values reviewed
by Goss-Custard (1980) for north temperate estuaries (22–45%), except in the highly improbable
case that Hydrobia constituted the bulk of the diet
for all species.
A recent study using exclosures to assess the
impact of bird predation and the presence of algal
mats on the abundance of intertidal invertebrates
confirmed that predation by birds was a negligible
factor in reducing prey abundances in this estuary
(Lopes et al., 2000). As Lopes et al.,’s study was
conducted during the spring migration period of
the birds, and lasted for just 2 months, their results
cannot be directly compared to ours, but does
further indicatate that prey depletion by birds is
probably small in the Mondego estuary.
In summary, the data indicate that competition
through interference and depletion on the mudflats
of the Mondego estuary was probably weak, or
entirely absent, during the study period. As a
consequence, the mudflats are likely to be able to
accommodate more birds over low tide. However
further research, probably involving individuals
behaviour-based modelling (Goss-Custard et al.,
2002), would be required to predict when food
competition would intensify to the point at which
some birds would die or leave the estuary.
This conclusion should not be taken to suggest,
however, that birds would be able to continue to
feed as well as they do at present were the salinas
to be reduced. Despite the fact that no evidence of
interference competition was found to occur in this
habitat at present, the salines are known to provide both alternative and supplementary feeding
for the estuarine birds (Múrias et al., 2002). Low
levels of competition on the mudflats does not
necessarily mean, therefore, that removing the
salinas would not make it more difficult for some
birds to obtain their daily requirements, especially
as their removal would reduce the time available
for foraging from 12 to 8 h. Thus, the loss of salines in the Mondego estuary may not be neutral in
terms of its effects on wintering birds even though
competition on the main intertidal feeding grounds
does seem to be weak or absent at the moment.
The next step is to model the system so that the
combined effect of the loss of important salines
feeding areas and the loss of feeding time on bird
fitness can be predicted (Goss-Custard et al.,
2002).
Acknowledgments
This work was supported by the Portuguese Research Board (FCT), through grants FMRH/BD/
331/93 and PRAXIS XXI/BD/5570/95 (TM),
PRAXIS XXI BM/3261/92-IG (JAC) and
PRAXIS XXI BM/7232/95 (RL). The authors are
indebted to all colleagues that helped in the fieldwork.
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